Breastfeeding prevalence in newborns of mothers with COVID-19: a systematic review

ABSTRACT Objectives: to compare exclusive breastfeeding prevalence versus artificial feeding in newborns of mothers with COVID-19. Methods: a systematic review of prevalence, according to JBI. Searches in PubMed®, Embase, CINAHL, LILACS and Web of Science™ databases in August 2021. Cross-sectional, longitudinal or cohort studies were selected, without language and time limitations that showed breastfeeding prevalence or that allowed calculation. Results: fifteen articles published in 2020 and 2021, cohort (60%) or cross-sectional (40%) were analyzed. The average of exclusive breastfeeding in mothers with COVID-19 was 56.76% (CI=39.90–72.88), and artificial breastfeeding, 43.23% (CI = 30.99 – 55.88), without statistically significant differences. Conclusions: despite the recommendations for maintaining breastfeeding, there was a reduction worldwide, when compared to periods prior to the pandemic. With advances in science, these rates have improved, showing the impact of evidence on practices. As limitations, study sources are cited. It is recommended to carry out new studies. PROSPERO registration CRD42021234486.


INTRODUCTION
Since the declaration of the COVID-19 pandemic, the population and the scientific community have been concerned about SARS-CoV-2 virus implications and consequences on specific practices and populations, such as breastfeeding of newborns (NBs) (1) .
The World Health Organization (WHO), the Ministry of Health (MOH) and the United Nations Children's Fund (UNICEF) recognize breastfeeding (BF) as a promoter and protector of child development, with recommendation to be practiced exclusively up to the sixth month of a child's life and, in the mixed form (concomitant with the introduction of food), up to two years or more (2) . Worldwide, 80% of NBs receive breast milk at some point in their lives (3) , but exclusive breastfeeding (EBF) prevalence at hospital discharge is 43% and up to six months of life for children is 41% (3) .
Human milk itself is an appropriate food for NBs and children, it completely meets nutritional needs up to the sixth month of life (4) , and has exclusive immune components (2,5) . Its nutritional composition and immune potential varies with gestational age, stage of lactation and health status of mother and child (4)(5) .
WHO data point to more than 450 million confirmed cases of SARS-CoV-2 infection and more than six million deaths worldwide due to the infection (6) , detected two years ago and with records of cases all over the world. Pregnant and puerperal women are classified as a risk group for infection, considered a priority in care and testing (7) .
In order to avoid possible post-childbirth contamination of NBs born to mothers with COVID-19, BF is recommended for mothers with mild symptoms, provided they use a surgical mask and rigorous hand hygiene (8) . Those with severe symptoms should be carefully assessed, but regardless, they should also be encouraged to express breast milk to start and maintain BF after the infection has resolved (7,(9)(10) . Expressed milk can be offered to NBs (7,(9)(10) .
This study considers BF prevalence among NBs born to women diagnosed with COVID-19, under the following justifications: COVID-19 is an emerging disease with a high magnitude and impact; the evidence of its effects during pregnancy and more specifically on NBs' health are still under investigation; the benefits of BF are already enshrined in literature; early weaning rates are high. Thus, maternal infection with COVID-19 is presumed to increase weaning prevalence.

OBJECTIVES
To compare EBF prevalence versus artificial BF in NBs of mothers with COVID-19.

Study design
This is a systematic review of prevalence. According to JBI, systematic reviews of prevalence or incidence data are becoming more important as policy makers realize the usefulness of summarizing this type of information. They aim to inform and update professionals in the social and health areas, public policy makers and consumers, for decision-making in health, particularly with regard to the current health burden and its projection for the future (11) .
The study was registered in the International Prospective Register of Systematic Reviews (PROSPERO) database, under registration CRD42021234486, structured according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) protocol (12) and JBI recommendations for systematic reviews prevalence (13) .
The review question was based on the Condition, Context and Population (CoCoPop) strategy, establishing Co (Condition) for BF prevalence, Co (Context), for the COVID-19 pandemic, and Pop (Population), for NBs of mothers with infection by COVID-19. Based on these definitions, the review question was: what is BF prevalence in NBs of mothers with COVID-19?

Data collection
The sources were consulted on August 2, 2021, held in the National Library of Medicine of the United States of America National Institutes of Health (PubMed ® ), Latin American and Caribbean Literature in Health Sciences (LILACS), Web of Science™, Excerpta Medica dataBASE (Embase) and Cumulative Index of Literature in Nursing and Related Sciences (CINAHL). The choice of databases was based on the number of indexed health articles. PubMed ® is a free search engine with access to the MEDLINE database, which registers important publications of American and world literature. CINAHL is a specific database for nursing and health sciences. LI-LACS contains production from Latin America and the Caribbean. Embase is an important biomedical database. Web of Science™ allows the query of other databases. The objective of the diversity of bases was to contemplate the world production on the theme.
The ). This strategy served as a standard for searches in other databases, with slight adaptations to the specific criteria of each database, as shown in Chart 1.

Selection criteria
Cross-sectional, longitudinal, cohort or follow-up studies were selected, without language or time frame limitations, that presented BF prevalence or that offered data that allowed the calculation of such measure (number of infants assessed and percentage of infants breastfeeding), regardless of whether assessed as a primary outcome. Studies were included that assessed BF prevalence in NBs at hospital discharge or up to 28 days after birth and children of mothers diagnosed with COVID-19 with laboratory confirmation (PCR positive) at the time of childbirth.

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Breastfeeding prevalence in newborns of mothers with COVID-19: a systematic review Ruiz MT, Oliveira KF, Azevedo NF, Paschoini MC, Rodrigues WF, Oliveira CJF, et al.
Articles with secondary data (reviews), editorials, expert opinions, letters to the editor or comments on articles, case studies (only case reported), guidelines, research protocols and consensus were excluded. The level of evidence was not considered an exclusion criterion, as this is a new topic.
Thus, 418 articles were identified in the five consulted databases. The PRISMA methodology was adopted (12) and is shown in Figure 1. Study selection was carried out independently by two researchers, and disagreements were resolved by consensus. Article analysis was carried out, in a first step, with the reading of title and abstract, followed by reading in full for the final selection of articles. The order of analyzed databases was PubMed ® , Embase, CINAHL, LILACS and Web of Science™. The order of exclusions followed the criteria: duplicate articles; study design inappropriate for the question -secondary data (reviews); editorials; expert opinions; letters to the editor or comments on articles; case studies (only case reported); guidelines, research protocols and consensus; and those who did not respond to the review question. Full texts were also selected in a paired and independent way.

Data analysis and treatment
In the first step, duplicate records were removed (n= 142). Initially, the choice of articles was based on analysis of titles and abstracts. At this stage, 243 articles were excluded, as 92 did not address the theme of BF or did not make it possible to determine its prevalence  and 151 did not have an adequate design for inclusion, of which, 67 were review studies on COVID-19 and maternal and child health. Then, 33 articles were read in full in an exhaustive way. One study was a review and the other 17 were excluded for the following reasons: they did not respond to the review response; lack of laboratory evidence of COVID-19; mixed samples with pregnant women without the disease; and infant assessment time (greater than 28 days). Thus, 15 studies were included in the review. The sequence of sources analyzed in the databases was PubMed ® , Embase, CINAHL, LILACS and Web of Science™. The JBI (13) appraisal tools were used to assess methodological quality and risk of bias of included studies. The assessment was carried out independently by two researchers with a doctoral degree. By consensus, the group of researchers determined the cut-off point for classifying articles: as high risk of bias (score less than 50%); as moderate risk of bias (scores between 50% and 70%); and as low risk of bias (scores above 70%). The critical assessment instruments were selected according to the methodology used in the assessed studies.
Data were synthesized by two pairs of independent researchers. A structured instrument was used to extract data from the studies, following the JBI guidelines (13) , which included article identification, country, study setting or context, participant characteristics, groups, measured outcomes and description of main results, when cohort studies were included. For prevalence studies, article identification, country, year/period of data collection, participant characteristics, conditions and methods of measurement and description of main results were assessed. The extracted information was tabulated for data synthesis, and the analysis of results was descriptive, presenting a summary of each primary study included in this review.
Data were stored in Microsoft ® Excel spreadsheets, and for analysis and visual display of the data, the RStudio program was used. Proportion meta-analysis was performed for BF prevalence and artificial, as well as for subgroup assessments (according to study design and year of publication). The General Package for Meta-Analysis "meta", version 4.9-5, was used to analyze the proportions of BF (maternal or artificial) by mothers with CO-VID-19, through the "meprop" command, being adjusted with the Freeman-Tukey double arcsine transformation (sm = "PFT"), and the random effect model was used for the determinations. The forest plot, or forest graph, was used to assess and represent the data. Study heterogeneity was assessed using the I 2 test statistic from Cochran's Q and the J number of analyzed studies.

RESULTS
Fifteen scientific articles were included in the analysis, nine (60%) of which were published in 2020 and six (40%) in 2021, 14 (93.3%) in English and one (0.7%) in Portuguese from Portugal. Most studies were cohorts (nine -60%), followed by cross-sectional studies (six -40%). The information is described in Chart 2.
BF at discharge. 52% (n = 40) were on EBF; 48% (n = 34) were on artificial feeding, 3% (n = 02) on artificial feeding and 45% (n = 32) on mixed feeding. Of these infants, only two had an indication for the use of a complementary formula to stabilize hypoglycemia. In neonatal return at 28 days of life, there was an increase in the EBF rate to 56% (n = 43).
The application of tools for assessing methodological quality and risk of bias from JBI Tools made it possible to identify low risk of bias (scores above 70%) in all cohort studies included, and, among cross-sectional studies, they were classified as low risk of bias. four bias studies (66.7%), moderate risk, one study (scores between 50 and 70%) and high risk (scores below 50%), one study.
The United States was the main country producing studies (six -40%); Italy and Spain had two publications included; a multicenter study with researchers from 31 countries was added to the review; and Peru, Portugal, Sweden and Turkey had one production each. Adding up all NBs, 4,391 children of mothers with proven COVID-19 diagnosis at the time of childbirth were assessed.
Due to the high heterogeneity presented by the studies included, the analysis was carried out by subgroups according to study design and year of publication. Figure 3 presents the analysis according to study design. In cohort studies, means of 52.43% (CI = 33.83 -70.70) and 47.57% for artificial feeding (CI = 29.30 -66.17) were observed. The heterogeneity observed in these studies was 99%. When analyzing cross-sectional studies, there was a reduction in heterogeneity to 87%, and the mean BF in these studies was 62.66% (CI = 48.94 -75.47), and artificial feeding was 37.44 % (CI = 24.53 -51.06).
It is noteworthy that, in cohort studies, the majority was carried out through review of medical records, electronic records and online surveys. Only one study (19) was carried out based on the follow-up assessment of NBs during hospitalization. Among the cross-sectional studies, the dyad was directly observed at the time of hospital discharge, except in one of them (23) , in which a multicentric online survey was carried out. Chart 2 (concluded) Characteristics of prevalence studies included in the review (n = 06)

Study Country
Year of data collection

DISCUSSION
The results of this review portray worrying rates of artificial feeding among NBs of mothers with COVID-19, but when more recent publications are analyzed, a reduction in these rates is evidenced.
Due to the importance of BF, these results are cause for concern, as the Center for Disease Control (CDC) and the Royal College of Obstetricians and Gynaecologists (RCOG) do not contraindicate BF, but only indicate the use of protective measures against the spread of SARS-CoV-2 (10,17) , due to the benefits of BF for mother and baby and lack of evidence to prove transmission through breast milk,     it should be encouraged (29)(30)(31)(32) . It should also be mentioned that NBs born to mothers with COVID-19 are already colonized with the virus, due to previous exposure to it during pregnancy (29)(30)(31)(32) . Despite the above notes, these same bodies and others agree to minimize the chances of exposure to the viral load with a contraindication for skin-to-skin contact, maintaining a distance of about two meters between the child's crib and the mother's bed until the infection is confirmed, frequently washing hands with soap and water and/or rubbing with 70% alcohol gel, using a disposable surgical mask and avoiding talking during feedings (8,10,(30)(31)(32)(33)(34) .
It is important to emphasize that the evidence points to the risk of transmission through direct and intimate contact (33) so that, with preventive measures and precautions, it is possible to safely establish milking and BF for asymptomatic and symptomatic mothers.
It is noteworthy that, during the pandemic period and infection duration, all nutrition options for NBs were justifiable, as it was an unknown disease; however, BF continues to be the most of Breastfeeding prevalence in newborns of mothers with COVID-19: a systematic review Ruiz MT, Oliveira KF, Azevedo NF, Paschoini MC, Rodrigues WF, Oliveira CJF, et al.
indicated for NBs, regardless of the infection. It reinforces the importance of guidance for mothers and families so that choices are conscious and based on scientific evidence (35) . These guidelines and decisions may start with COVID-19 diagnosis, but have, in the period of hospitalization after birth, a strategic moment, with direct influences on the establishment of EBF (33) . A survey (36) carried out in American hospitals pointed out that, from July to August 2020, of the 1,344 participating institutions, 66.9% encouraged BF with precautions; 20.1% left it as the woman's choice, without offering support, to avoid health workers' exposure time; 12.7% encouraged milking; and 0.2% prescribed artificial feeding (formula). It was highlighted that the reduction in BF rates can be caused by the separation/distance between mother and child, early hospital discharge (hospitalization time less than 48 hours) and the reduction of support both during hospitalization and at home (36) .
A study (37) carried out in Italy showed a 15% reduction in BF rates, with a higher prevalence of formula use during the pandemic period. Data were statistically significant when compared to the rates presented in the year before the pandemic. Additionally, higher scores of depressive symptoms and anhedonia were observed in women who did not breastfeed their children, indicating possible long-term outcomes in maternal mental health.
A series of 22 cases described in Spain also showed that 90% of mothers infected with COVID-19 chose to breastfeed their children with precautions. However, during follow-up, it was found that, at two months, only 77% continued BF and, in all cases, no NB was infected with SARS-CoV-2 (38) . This result suggests that longitudinal support for nursing mothers is essential to deal with the difficulties and doubts they may be experiencing (38) .
An online survey (39) with mothers with children under one year old in England showed contradictory data. Thus, 41.8% felt that BF was protected by the pandemic, as they were able to stay at home with children, but 27% found barriers to seeking support and weaned their children early. Women with low education and of black color were more prone to early weaning during the pandemic, showing social inequalities in access to BF protection resources. According to the authors, reduced support, face-toface contact with health professionals, mother-baby separation, confinement and reduced social support (family, friends and communities) can contribute to high weaning rates (39) , and the long-term impacts of increasing these rates are yet to be known.
A study (40) carried out with 18 infected postpartum women in the United States pointed out that the Polymerase Chain Reaction (PCR) was positive in only one breast milk sample from a woman who was on the first day of infection. Following the analysis on the 2 nd , 12 th and 41 st days, the PCR was negative. The positive sample, when subjected to pasteurization (heating at 62.5°C for 30 minutes and subsequent cooling to 4°C), was tested and proved negative. The authors pointed out that BF may not be a source of infection for infants and that the pasteurization process inactivates the virus (40) .
In a Chinese study (41) , breast milk samples were collected from a mother with positive PCR for COVID-19, weekly, for a period of one month. Detection of immunoglobulin G (IgG) and immunoglobulin A (IgA) was observed, with progressive increase in milk and concomitant reduction of IgG in infants' blood until it became negative. Infants maintained negative PCR and received breast milk from birth. The authors point to the potential of immune protection of milk for NBs, suggesting that new studies be carried out to prove it (41) .
UNICEF data from 2018 (42) showed that 95% of infants worldwide received breast milk at least once in their lives, with the use of formula (artificial feeding) being more frequent in developed countries (one in five infants), compared to developing countries (one in 25). However, the same report points out that, in the same countries of origin of the reviewed studies (United States, Spain, Italy, Peru, Portugal, Sweden and Turkey), in 2018, BF rates ranged from 74.4 to 98.7 % (42) .
Two aspects related to the results presented must be highlighted. The first concerns the study design, as there was a predominance of data collected from medical records, online surveys or electronic systems in the cohorts carried out. The investigation of printed and electronic medical records allows knowing patients' health conditions, but the observation relates health conditions to care and their intersections, in addition to making it possible to know the relationship of individuals with their family, with other people, with the institution, their perspectives, expectations and opinions, providing greater detail. The use of more than one method (triangulation) makes it possible to assess a reality from different perspectives and with a lower risk of bias (43) .
The second relates to the year of production of the publications. The reduction of artificial feeding with the advancement of science is remarkable. It is noteworthy that, after one year of the pandemic, seven aspects of progress were observed: collaboration between teams; genetic sequencing of the virus; development of different diagnostic tests; vaccine development and distribution; adjuvant treatments; greater compliance with hygiene practices by the population; and the importance of scientific research to control the pandemic (44) .

Study limitations
As limitations, the predominance of data collected from medical records, online surveys or electronic systems in the cohorts carried out stands out, which can compromise the results, due to the increased risk of response bias, constituting a limitation regarding the generalization of results. Furthermore, because it is a new disease, with a rapid update of the literature and an increase in the number of cases, divergent results may appear on the subject.

Contributions to nursing and health
Given the evidence presented, it appears that BF should be a choice of the mother and family, however, given the risks of infection and the benefits of BF, even in the presence of infection, it is strongly recommended to maintain BF with precautions. It should also be noted that the long-term impact of the increase in early weaning rates on child health and public health is unknown, requiring studies on the subject.
It is up to health professionals to offer support in this decisionmaking and development of children's feeding practice. Every woman and family have the right to receive this support, which 12 of Breastfeeding prevalence in newborns of mothers with COVID-19: a systematic review Ruiz MT, Oliveira KF, Azevedo NF, Paschoini MC, Rodrigues WF, Oliveira CJF, et al.
includes current and comprehensible information regarding the specificities of understanding and possibilities.

CONCLUSIONS
EBF prevalence in NBs of mothers diagnosed with COVID-19 (56.76%) was higher than the mean for artificial feeding (43.24%). However, despite the recommendations for maintaining BF, even in the face of infection, there was a reduction in their rates, when compared to periods prior to the pandemic, which ranged from 74.4 to 98.7% in the producing countries cited in this review.
More recent studies point to a reduction in artificial feeding rates, showing the impact of evidence on practices. It is suggested to monitor the impact of weaning in the short and long term on the overall health of children born during the pandemic.